The complex structure of Fomes fomentarius represents an architectural design for high-performance ultralightweight materials

Abstract

High strength, hardness, and fracture toughness are mechanical properties that are not commonly associated with the fleshy body of a fungus. Here, we show with detailed structural, chemical, and mechanical characterization that Fomes fomentarius is an exception, and its architectural design is a source of inspiration for an emerging class of ultralightweight high-performance materials. Our findings reveal that F. fomentarius is a functionally graded material with three distinct layers that undergo multiscale hierarchical self-assembly. Mycelium is the primary component in all layers. However, in each layer, mycelium exhibits a very distinct microstructure with unique preferential orientation, aspect ratio, density, and branch length. We also show that an extracellular matrix acts as a reinforcing adhesive that differs in each layer in terms of quantity, polymeric content, and interconnectivity. These findings demonstrate how the synergistic interplay of the aforementioned features results in distinct mechanical properties for each layer.

Fig. 1.. The ultra-architecture of F. fomentarius used in this study.

The x-ray 2D projections of the three main regions crust (I), context (II), and H. tubes (III) and their corresponding interfaces (circles) are shown. The imaginary yellow dashed line stretches from the posterior to the anterior region, indicating the boundary between the context and the H. tube layer.

Fig. 2.. A closer look at the three distinct main regions of the fruiting body using x-ray μCT and high-resolution SEM.

(A) μCT and SEM images of the cross section and surface of the crust. (B) μCT and SEM image of the context. (C) X-Y-Z CT slices and 3D reconstruction of H. tubes at various rotating positions. (C) also demonstrates an SEM image of the cross section. The internal region and the tube walls are indicated by yellow dashed lines. (D) Calculated percentage porosity from μCT slides for all three regions. The plot also demonstrates the calculated density for each layer. (E and F) Calculated branch length of the hyphae in the context as well as the H. tubes.

Fig. 3.. Hymenophore tubes form the largest area in the F. fomentarius.

(A) 3D reconstruction of H. tubes (golden brown) and the calculated empty space of each tube (blue). The air pockets are shown from the top and side views. (B) The calculated diameter of the H. tubes for five different zones and the representative μCT slices. (C) Interface between the context and H. tubes (corresponding to zone I) demonstrating preferential alignment of the mycelium network in the context region before assembling into growth cones, which ultimately templates the formation of the tubes (the individual cone indicated with the blue arrow, tube with the red arrow, and the array of the growth cone with the green square bracket). (D) A closer look at the H. tube’s surface where the spores are released (most active region of the fruiting bodies), illustrating the primary and tertiary mycelium (corresponding to zone V).

Fig. 4.. The spectral analysis demonstrates distinct structural and chemical differences between the crust, context, and H. tubes.

(A) X-Y CT slice of the crust–context–H. tube interface and the 3D reconstruction for the same region. (A) also demonstrates 92 simultaneous WAXS/SAXS measurements from the exterior to the interior side of the corresponding specimen. (A) also shows the calculated HOP by azimuthal integration of 111 arc as in (C). (B) High-resolution SEM imaging from each layer. (C) 1D and 2D WAXS/SAXS measurements corresponding to each layer. (D) ATR-FTIR measurement of the crust, context, and H. tubes corresponding to the layers imaged in (B).

Fig. 5.. Cell walls of the mycelium present in each layer exhibit distinct chemical composition and structural organization.

(A) ¹H proton-detected [cross-polarization (CP)based] 2D ¹H-¹³C correlation spectrum (with back CP of 200 μs) of the crust, context, and H-tubes. (B) Relative abundance of polysaccharides present in each layer calculated from the peak integration using Topspin. (C) Schematic representation of the mycelium’s cell wall in the crust, context, and H. tubes. The major components, their interconnectivity, and their approximate position with respect to the cell membrane are shown.

Fig. 6.. Mechanical characterization of each layer.

(A) Representative tensile stress-strain curves for the context and the H. tubes. Mean values ± SD (n = 8) for stress, strain, Young’s modulus, and toughness are also shown. (B and C) Ashby plots comparing different types of natural and synthetic materials with the context and H. tube regions. Young’s modulus versus density, as well as strength versus density. (D) SEM images were also taken from the fractured surfaces after tensile tests to better identify mechanical response and failure mechanisms.

Fig. 7.. The preferential orientation of mycelium in the longitudinal direction increased the mechanical performance of the materials.

(A and B) Representative compression stress-strain curves for the context and H. tubes for specimens cut longitudinally and laterally. (A) and (B) also demonstrate high-resolution SEM images of the specimens before the compression test, illustrating the longitudinal orientation of the mycelium in the context and H. tubes. A falsely colored SEM image shows the presence of extracellular matrix that embedded and glued together the mycelium in the H. tube, whereas no extracellular matrix can be seen in the case of the context. (C) X-Y CT slice of the H. tubes after compression test showing that the material follows sequential energy dissipating failure. This includes bending, crack initiation, and, lastly, crack propagation for the lateral cut. (D) X-Y CT slice of the H. tubes cut longitudinally after compression test showing how the material dissipates energy through buckling effect. (E) Indentation modulus for the crust, context, and H. tubes.